Bioactive Compounds Obtained from Oilseed By-Products with Subcritical Fluids: Effects on Fusarium verticillioides Growth

Abstract

Recovery of bioactive compounds from wastes is gaining interest because they could add value to by-products arising from, for example, the oil extraction processes. In this work, green solvent extraction (water/ethanol under sub-critical conditions) was used to obtain bioactive compounds from peanut, sesame and pistachio agro-industrial by-products. Extracts were analyzed in their overall chemical composition and tested on growth, ergosterol and fumonisin FB1 production by Fusarium verticillioides. The effects of the extracts on fungal growth rate and biochemical markers were not univocal, and could be associated to differences in their chemical profiles. Extracts obtained from peanut skin—composed mainly by monomeric and dimeric flavonoids—caused significant reductions in fungal growth rate but increased FB1 production. Extracts from sesame seeds—dominated by furofuran-type lignans—did not have a clear inhibitory effect on growth rate but strongly reduced both FB1 and ergosterol production. Extracts from pistachio nuts—characterized by monomeric flavonoids and gallic acid derivatives—showed minor effects on both fungal growth rate and biochemical markers. Sub-critical fluid extraction of peanut skin and defatted sesame seeds may provide an efficient method to obtain extracts rich in phenolic and lignan compounds with potential use as antifungal agents.

Graphic Abstract

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

FB1 :

Fumonisin B1

GA:

Galic acid

HPLC–ESI–MS/MS:

High pressure liquid chromatography–electrospray ionization–mass spectroscopy

PNC:

Pistachio nuts cake

PS:

Peanut skin

SSC:

Sesame seed cake

SFE:

Sub-critical fluid extraction

TPC:

Total phenol content

References

  1. 1.

    Banerjee, J., Singh, R., Vijayaraghavan, R., MacFarlane, D., Patti, A.F., Arora, A.: Bioactives from fruit processing wastes: green approaches to valuable chemicals. Food Chem. 225, 10–22 (2017)

    Google Scholar 

  2. 2.

    Lai, W.T., Khong, N.M.H., Lim, S.S., Hee, Y.Y., Sim, B.Y., Lau, K.Y., Lai, O.M.: A review: modified agricultural by-products for the development and fortification of food products and nutraceuticals. Trends Food Sci. Technol. 59, 148–160 (2016)

    Google Scholar 

  3. 3.

    Nazzaro, F., Fratianni, F., Ombra, M.N., D’Acierno, A., Coppola, R.: Recovery of biomolecules of high benefit from food waste. Curr. Opin. Food Sci. 22, 43–54 (2018)

    Google Scholar 

  4. 4.

    Sunil, L., Appaiah, P., Prasanth Kumar, P.K., Gopala Krishna, A.G.: Preparation of food supplements from oilseed cakes. J. Food Sci. Technol. 52, 2998–3005 (2014)

    Google Scholar 

  5. 5.

    Sarkis, J.R., Correa, A.P.F., Michel, I., Brandeli, A., Tessaro, I.C., Marczak, L.D.F.: Evaluation of the phenolic content and antioxidant activity of different seed and nut cakes from the edible oil industry. J. Am. Oil Chem. Soc. 91, 1773–1782 (2014)

    Google Scholar 

  6. 6.

    Terpinc, P., Ceh, B., Ulrih, N.P., Abramoviˇc, H.: Studies of the correlation between antioxidant properties and the total phenolic content of different oil cake extracts. Ind. Crops Prod. 39, 210–217 (2012)

    Google Scholar 

  7. 7.

    Ramachandran, S., Singh, S.K., Larroche, C., Soccol, C.R., Pandey, A.: Oil cakes and their biotechnological applications—a review. Bioresour. Technol. 98, 2000–2009 (2007)

    Google Scholar 

  8. 8.

    Meriles, J.M., Giorda, L.M., Maestri, D.M.: Effect of planting date on Fusarium spp. and Diaporthe/Phomopsis complex incidence and its relationship with soybean seed quality. J. Phytopathol. 150, 606–610 (2002)

    Google Scholar 

  9. 9.

    IARC: International Agency for Research on Cancer.: IARC Monographs on the Evaluation of the Carcinogenic Risks to Humans: Some Traditional Herbal Medicines, Some Mycotoxins, Naphthalene and Styrene, vol. 82, pp. 301–366. International Agency for Research on Cancer, Lyon (2002)

    Google Scholar 

  10. 10.

    Agrios, G.: Plant Pathol, 5th edn. Elsevier Academic Press, Nueva York (2005)

    Google Scholar 

  11. 11.

    Błaszczak-Świątkiewicz, K., Sikora, J., Szymański, J., Danilewicz, M., Mikiciuk-Olasik, E.: Biological evaluation of the toxicity and the cell cycle interruption by some benzimidazole derivatives. Tumor Biol. 37, 11135–11145 (2016)

    Google Scholar 

  12. 12.

    Seiber, J.N., Coats, J., Duke, S.O., Gross, A.D.: Biopesticides: state of the art and future opportunities. J. Agric. Food Chem. 62, 11613–11619 (2014)

    Google Scholar 

  13. 13.

    Barral, B., Chillet, M., Minier, J., Lechaudel, M., Schorrgalindo, S.: Evaluating the response to Fusarium ananatum inoculation and antifungal activity of phenolic acids in pineapple. Fungal Biol. 121, 1045–1053 (2017)

    Google Scholar 

  14. 14.

    Wang, S., Zheng, Y., Xiang, F., Li, S., Yang, G.: Antifungal activity of Momordica charantia seed extracts toward the pathogenic fungus Fusarium solani L. J. Food Drug Anal. 24, 881–887 (2016)

    Google Scholar 

  15. 15.

    Brado Avanço, G., Dias Ferreira, F., Silva Bomfim, N., De Souza, A., Rodrigues dos Santos, P., Peralta, R.M., Brugnari, T., Mallmann, C.A., de Abreu, Alves, Filho, B., Graton Mikcha, J.M., Machinski, M.: Curcuma longa L. essential oil composition, antioxidant effect, and effect on Fusarium verticillioides and fumonisin production. Food Control 73, 806–813 (2017)

    Google Scholar 

  16. 16.

    Dambolena, J.S., López, A.G., Meriles, J.M., Rubinstein, H.R., Zygadlo, J.A.: Inhibitory effect of 10 natural phenolic compounds on Fusarium verticillioides. A structure property activity relationship study. Food Control 28, 63–70 (2012)

    Google Scholar 

  17. 17.

    Da Silva, Bomfim N., Polis Nakassugi, L., Faggion Pinheiro Oliveira, J., Yumie Kohiyama, C., Aparecida, S., Mossini, G., Grespan, R., Botião Nerilo, S., Mallmann, C.A., Abreu Filho, B.A., Machinski, M.: Antifungal activity and inhibition of fumonisin production by Rosmarinus officinalis L. essential oil in Fusarium verticillioides (Sacc.) Nirenberg. Food Chem. 166, 330–336 (2015)

    Google Scholar 

  18. 18.

    Bodoira, R., Velez, A., Andreatta, A.E., Martinez, M., Maestri, D.: Extraction of bioactive compounds from sesame (Sesamum indicum L.) defatted seeds using water and ethanol under sub-critical conditions. Food Chem. 237, 114–120 (2017)

    Google Scholar 

  19. 19.

    Ben Othman, S., Katsuno, N., Kanamaru, Y., Yabe, T.: Water-soluble extracts from defatted sesame seed flour show antioxidant activity in vitro. Food Chem. 175, 306–314 (2015)

    Google Scholar 

  20. 20.

    Esmaeilzadeh, B.S., Sharifi, M., Behmanesh, M., Safaie, N., Murata, J., Araki, R., Yamagaki, T., Satake, H.: Time-course changes in fungal elicitor-induced lignan synthesis and expression of the relevant genes in cell cultures of Linum album. J. Plant Physiol. 169, 487–491 (2012)

    Google Scholar 

  21. 21.

    Kulik, T., Busko, M., Pszczółkowska, A., Perkowsk, J., Okorski, A.: Plant lignans inhibit growth and trichothecene biosynthesis in Fusarium graminearum Lett. Appl. Microbiol. 59(99), 107 (2014)

    Google Scholar 

  22. 22.

    Barbary, O.M., El-Sohaimy, S.A., El-Saadani, M.A., Zeitoun, A.M.A.: Antioxidant, antimicrobial and anti-HCV activities of lignan extracted from flaxseed. Res. J. Agric. Biol. Sci. 6, 247–256 (2010)

    Google Scholar 

  23. 23.

    Nishiwaki, H., Nakazaki, S., Akiyama, K., Yamauchi, S.: Structure-antifungal activity relationship of fluorinated dihydroguaiaretic acid derivatives and preventive activity against Alternaria alternata Japanese pear pathotype. J. Agric. Food Chem. 65, 6701–6707 (2017)

    Google Scholar 

  24. 24.

    Ma, Y.Y., Cagnazzo, A.K., Kerr, W.L., Amarowicz, R., Swanson, R.B., Pegg, R.B.: Separation and characterization of phenolic compounds from dry-blanched peanut skins by liquid chromatography–electrospray ionization mass spectrometry. J. Chromatogr. A 1356, 64–81 (2014)

    Google Scholar 

  25. 25.

    Bodoira, R., Rossi, Y., Montenegro, M., Maestri, D., Velez, A.: Extraction of antioxidant polyphenolic compounds from peanut skin using water-ethanol at high pressure and temperature conditions. J. Supercrit. Fluid 128, 57–65 (2017)

    Google Scholar 

  26. 26.

    Pizzolitto, R.P., Dambolena, J.S., Zunino, M.P., Larrauri, M., Grosso, N.R., Nepote, V., Dalcero, A.M., Zygadlo, J.A.: Activity of natural compounds from peanut skins on Fusarium verticillioides growth and fumonisin B1 production. Ind. Crops Prod. 47, 286–290 (2013)

    Google Scholar 

  27. 27.

    Sarnoski, P., Boyer, R., O’Keefe, S.F.: Application of proanthocyanidins from peanut skins as a natural yeast inhibitory agent. J. Food Sci. 77, 242–249 (2012)

    Google Scholar 

  28. 28.

    Rajaei, A., Barzegar, M., Mobarez, A.M., Sahari, M.A., Esfahani, Z.H.: Antioxidant, anti-microbial and antimutagenicity activities of pistachio (Pistachio vera) green hull extract. Food Chem. Toxicol. 48, 107–112 (2010)

    Google Scholar 

  29. 29.

    Chemat, F., Rombaut, N., Meullemiestre, A., Turk, M., Perino, S., Fabiano-Tixier, A.S., Abert-Vian, M.: Review of green food processing techniques. Preservation, transformation and extraction. Innov Food Sci. Emerg. Technol. 41, 357–377 (2017)

    Google Scholar 

  30. 30.

    Martínez, M.M., Bordón, M.G., Lallana, R.L., Ribotta, P.D., Maestri, D.M.: Optimization of sesame oil extraction by screw-pressing at low temperature. Food Bioprocess Tech. 10, 1113–1121 (2017)

    Google Scholar 

  31. 31.

    Singleton, V.L., Orthofer, R., Lamuela-Raventós, R.M.: Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 299, 152–178 (1999)

    Google Scholar 

  32. 32.

    Ersan, S., Ustundag, O.G., Carle, R., Schweiggert, R.F.: Identification of phenolic compounds in red and green pistachio (Pistacia vera L.) hulls (exo- and mesocarp) by HPLC-DAD-ESI-(HR)-MS. J. Agric. Food Chem. 64, 5334–5344 (2016)

    Google Scholar 

  33. 33.

    Leslie, J.F., Plattner, R.D., Desjardins, A.E., Klittich, C.J.: Fumonisin B1 production by strains from different mating populations of Gibberella fujikuroi (Fusarium section Liseola). Phytopathology 82, 341–345 (1992)

    Google Scholar 

  34. 34.

    Shephard, G.S., Sydenham, E.W., Thiel, P.G., Gelderblom, W.C.A.: Quantitative determination of fumonisin B1 and B2 by high-performance liquid chromatography with fluorescence detection. J. Liq. Chromatogr. 13, 2077–2087 (1990)

    Google Scholar 

  35. 35.

    Dambolena, J.S., López, A.G., Canepa, M.C., Theumer, M.G., Zygadlo, J.A., Rubinstein, H.R.: Inhibitory effect of cyclic terpenes (limonene, menthol, menthone and thymol) on Fusarium verticillioides MRC 826 growth and fumonisin B1 biosynthesis. Toxicon 51, 37–44 (2008)

    Google Scholar 

  36. 36.

    Sichetti Munekata, P.E., Paseto Fernandes, R.P., Pires de Melo, M., Trindade, M.A., Lorenzo, J.M.: Influence of peanut skin extract on shelf-life of sheep patties. Asian Pac. J. Trop. Med. 6, 586–596 (2016)

    Google Scholar 

  37. 37.

    Sarnoski, P.J., Johnson, J.V., Reed, K.A., Tanko, J.M., O’Keefe, S.F.: Separation and characterisation of proanthocyanidins in Virginia type peanut skins by LC–MS. Food Chem. 131, 927–939 (2012)

    Google Scholar 

  38. 38.

    Moazzami, A.A., Andersson, R.E., Kamal-Eldin, A.: HPLC analysis of sesaminol glucosides in sesame seeds. J. Agric. Food Chem. 54, 633–638 (2007)

    Google Scholar 

  39. 39.

    Dar, A.A., Arumugam, N.: Lignans of sesame: Purification methods, biological activities and biosynthesis—a review. Bioorg. Chem. 50, 1–10 (2013)

    Google Scholar 

  40. 40.

    Nadeem, M., Situ, C., Mahmud, A., Khalique, A., Imran, M., Rahman, F., Khan, S.: Antioxidant activity of sesame (Sesamum indicum L.) cake extract for the stabilization of olein based butter. J. Am. Oil Chem. Soc. 91, 967–977 (2014)

    Google Scholar 

  41. 41.

    Shan, B., Cai, Y.Z., Brooks, J.D., Corke, H.: Antibacterial properties of Polygonum cuspidatum roots and their major bioactive constituents. Food Chem. 109, 530–537 (2008)

    Google Scholar 

  42. 42.

    Hwang, B., Lee, J., Liu, Q., Woo, E., Lee, D.G.: Antifungal effect of (+)-pinoresinol isolated from Sambucus williamsii. Molecules 15, 3507–3516 (2010)

    Google Scholar 

  43. 43.

    Céspedes, C.L., Guillermo Avila, J., García, A.M., Becerra, J., Flores, C., Aqueveque, P., Bittner, M., Hoeneisen, M., Martinez, M., Silva, M.: Antifungal and antibacterial activities of Araucaria araucana (Mol.) K. Koch heartwood lignans. Zeitschrift für Naturforschung C 61, 35–43 (2006)

    Google Scholar 

  44. 44.

    Reynoso, M., Torres, A., Ramírez, M.L., Rodríguez, M., Chulze, S., Magan, N.: Efficacy of antioxidant mixtures on growth, fumonisins production and hydrolyticenzyme production by Fusarium verticillioides and F. proliferatum in vitro on maize-based media. Mycol. Res. 106, 1093–1099 (2002)

    Google Scholar 

  45. 45.

    Bendaha, H., Yu, L., Touzani, R., Souane, R., Giaever, G., Nislowc, C., Boone, C., El Kadiri, S., Brownb, G.W., Bellaoui, M.: New azole antifungal agents with novel modes of action: synthesis and biological studies of new tridentate ligands based on pyrazole and triazole. Eur. J. Med. Chem. 46, 4117–4124 (2011)

    Google Scholar 

Download references

Acknowledgements

Financial support was provided from CONICET, FONCYT, SECyT-UNC and MINCyT-Córdoba. We are indebted to Romina Di Paola Naranjo (ICYTAC-CONICET) and Damián Barrionuevo (IMBIV-CONICET-UNC) for their assistance in HPLC–ESI–MS/MS and HPLC–UV analyses.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jimena Herrera.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 25 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bodoira, R., Velez, A., Maestri, D. et al. Bioactive Compounds Obtained from Oilseed By-Products with Subcritical Fluids: Effects on Fusarium verticillioides Growth. Waste Biomass Valor 11, 5913–5924 (2020). https://doi.org/10.1007/s12649-019-00839-y

Download citation

Keywords

  • Food oil industry wastes
  • Bioactive compounds
  • Natural antifungal
  • Subcritical extraction